The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress

Abstract Background Aluminum (Al) toxicity inhibits plant growth and alters gene expression and metabolite profiles. However, the molecular mechanisms underlying the effects of Al toxicity on peanut plants remain unclear. Transcriptome and metabolome analyses were conducted to investigate the respon...

Full description

Saved in:
Bibliographic Details
Main Authors: Jianning Shi, Yishuang Zhou, Shaoxia Yang, Yingbin Xue, Yanyan Wang, Hanqiao Hu, Ying Liu
Format: Article
Language:English
Published: BMC 2025-04-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-025-06460-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849737320198045696
author Jianning Shi
Yishuang Zhou
Shaoxia Yang
Yingbin Xue
Yanyan Wang
Hanqiao Hu
Ying Liu
author_facet Jianning Shi
Yishuang Zhou
Shaoxia Yang
Yingbin Xue
Yanyan Wang
Hanqiao Hu
Ying Liu
author_sort Jianning Shi
collection DOAJ
description Abstract Background Aluminum (Al) toxicity inhibits plant growth and alters gene expression and metabolite profiles. However, the molecular mechanisms underlying the effects of Al toxicity on peanut plants remain unclear. Transcriptome and metabolome analyses were conducted to investigate the responses of peanut leaves and roots to Al toxicity. Results Al toxicity significantly inhibited peanut growth, disrupted antioxidant enzyme systems in roots and leaves, and impaired nutrient absorption. Under Al toxicity stress, the content of indole-3-acetic acid-aspartate (IAA-Asp) decreased by 23.94% in leaves but increased by 12.91% in roots. Methyl jasmonate (MeJA) levels in leaves increased dramatically by 2642.86%. Methyl salicylate (MeSA) content in leaves and roots increased significantly by 140.00% and 472.22%, respectively. Conversely, isopentenyl adenosine (IPA) content decreased by 78.95% in leaves and 20.66% in roots. Transcriptome analysis identified 5831 differentially expressed genes (DEGs) in leaves and 6405 DEGs in roots, whereas metabolomics analysis revealed 210 differentially accumulated metabolites (DAMs) in leaves and 240 DAMs in roots. Under Al toxicity stress, both leaves and roots were significantly enriched in the “linoleic acid metabolism” pathway. Genes such as lipoxygenase LOX1-5 and LOX2S were differentially expressed, and metabolites, including linoleic acid and its oxidized derivatives, were differentially accumulated, mitigating oxidative stress. Conclusions This study elaborates on the potential complex physiological and molecular mechanisms of peanuts under aluminum toxicity stress, and highlights the importance of linoleic acid metabolism in coping with aluminum toxicity. These findings enhance our understanding of the impact of aluminum toxicity on peanut development and the response of key metabolic pathways, providing potential molecular targets for genetic engineering to improve crop resistance to aluminum stress.
format Article
id doaj-art-a67d481d232043dfa10d369078cc2002
institution DOAJ
issn 1471-2229
language English
publishDate 2025-04-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj-art-a67d481d232043dfa10d369078cc20022025-08-20T03:06:57ZengBMCBMC Plant Biology1471-22292025-04-0125111810.1186/s12870-025-06460-7The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stressJianning Shi0Yishuang Zhou1Shaoxia Yang2Yingbin Xue3Yanyan Wang4Hanqiao Hu5Ying Liu6Department of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityDepartment of Agronomy, College of Coastal Agricultural Sciences, Guangdong Ocean UniversityAbstract Background Aluminum (Al) toxicity inhibits plant growth and alters gene expression and metabolite profiles. However, the molecular mechanisms underlying the effects of Al toxicity on peanut plants remain unclear. Transcriptome and metabolome analyses were conducted to investigate the responses of peanut leaves and roots to Al toxicity. Results Al toxicity significantly inhibited peanut growth, disrupted antioxidant enzyme systems in roots and leaves, and impaired nutrient absorption. Under Al toxicity stress, the content of indole-3-acetic acid-aspartate (IAA-Asp) decreased by 23.94% in leaves but increased by 12.91% in roots. Methyl jasmonate (MeJA) levels in leaves increased dramatically by 2642.86%. Methyl salicylate (MeSA) content in leaves and roots increased significantly by 140.00% and 472.22%, respectively. Conversely, isopentenyl adenosine (IPA) content decreased by 78.95% in leaves and 20.66% in roots. Transcriptome analysis identified 5831 differentially expressed genes (DEGs) in leaves and 6405 DEGs in roots, whereas metabolomics analysis revealed 210 differentially accumulated metabolites (DAMs) in leaves and 240 DAMs in roots. Under Al toxicity stress, both leaves and roots were significantly enriched in the “linoleic acid metabolism” pathway. Genes such as lipoxygenase LOX1-5 and LOX2S were differentially expressed, and metabolites, including linoleic acid and its oxidized derivatives, were differentially accumulated, mitigating oxidative stress. Conclusions This study elaborates on the potential complex physiological and molecular mechanisms of peanuts under aluminum toxicity stress, and highlights the importance of linoleic acid metabolism in coping with aluminum toxicity. These findings enhance our understanding of the impact of aluminum toxicity on peanut development and the response of key metabolic pathways, providing potential molecular targets for genetic engineering to improve crop resistance to aluminum stress.https://doi.org/10.1186/s12870-025-06460-7Arachis hypogaeaAl toxicity stressTranscriptomicsMetabolomicsMolecular mechanism
spellingShingle Jianning Shi
Yishuang Zhou
Shaoxia Yang
Yingbin Xue
Yanyan Wang
Hanqiao Hu
Ying Liu
The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
BMC Plant Biology
Arachis hypogaea
Al toxicity stress
Transcriptomics
Metabolomics
Molecular mechanism
title The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
title_full The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
title_fullStr The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
title_full_unstemmed The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
title_short The key metabolic pathway of roots and leaves responses in Arachis hypogaea under Al toxicity stress
title_sort key metabolic pathway of roots and leaves responses in arachis hypogaea under al toxicity stress
topic Arachis hypogaea
Al toxicity stress
Transcriptomics
Metabolomics
Molecular mechanism
url https://doi.org/10.1186/s12870-025-06460-7
work_keys_str_mv AT jianningshi thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yishuangzhou thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT shaoxiayang thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yingbinxue thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yanyanwang thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT hanqiaohu thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yingliu thekeymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT jianningshi keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yishuangzhou keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT shaoxiayang keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yingbinxue keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yanyanwang keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT hanqiaohu keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress
AT yingliu keymetabolicpathwayofrootsandleavesresponsesinarachishypogaeaunderaltoxicitystress